Genus-Wide Transcriptional Landscapes Reveal Correlated Gene Networks Underlying Microevolutionary Divergence in Diatoms.

Nathan G Walworth, Josh L Espinoza, Phoebe A Argyle, Jana Hinners, Naomi M Levine, Martina A Doblin, Chris L Dupont, Sinéad Collins

Journal: Molecular biology and evolution 2023;40(10):msad218

PMID: 37874344

Abstract

Marine microbes like diatoms make up the base of marine food webs and drive global nutrient cycles. Despite their key roles in ecology, biogeochemistry, and biotechnology, we have limited empirical data on how forces other than adaptation may drive diatom diversification, especially in the absence of environmental change. One key feature of diatom populations is frequent extreme reductions in population size, which can occur both in situ and ex situ as part of bloom-and-bust growth dynamics. This can drive divergence between closely related lineages, even in the absence of environmental differences. Here, we combine experimental evolution and transcriptome landscapes (t-scapes) to reveal repeated evolutionary divergence within several species of diatoms in a constant environment. We show that most of the transcriptional divergence can be captured on a reduced set of axes, and that repeatable evolution can occur along a single major axis of variation defined by core ortholog expression comprising common metabolic pathways. Previous work has associated specific transcriptional changes in gene networks with environmental factors. Here, we find that these same gene networks diverge in the absence of environmental change, suggesting these pathways may be central in generating phenotypic diversity as a result of both selective and random evolutionary forces. If this is the case, these genes and the functions they encode may represent universal axes of variation. Such axes that capture suites of interacting transcriptional changes during diversification improve our understanding of both global patterns in local adaptation and microdiversity, as well as evolutionary forces shaping algal cultivation.

© The Author(s) 2023. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution.

Address: Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089-0371, USA.; J.Craig Venter Institute, La Jolla, CA 92037, USA.; Climate Change Cluster, University of Technology Sydney, Sydney, New South Wales 2007, Australia.; School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3FL, UK.; Helmholtz-Zentrum Hereon, 21502 Geesthacht, Germany.
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